Revalidatiewetenschappen en Kinesitherapie Academiejaar 2014-2015

The role of core stability in sustaining high speed

running hamstring injuries in male soccer players

Masterproef voorgelegd tot het behalen van de graad van Master of Science in de Revalidatiewetenschappen en Kinesitherapie

Bonte Jelle De Brabander Joachim

Promotor: Prof. Dr. D. Van Tiggelen

Copromotor: Schuermans Joke

Word of thanks

We would like to thank the people who helped directly or indirectly with the achievement of this

article. First of all, we want to thank the soccer players who participated in this study. They all had to

make several hours of their time free to come to the testing location and do at least 12 maximal

accelerations. We definitely want to express our gratitude to our copromotor, Joke Schuermans, to

give straight and immediately feedback. We could always contact her for questions and she always

stayed calm when something went wrong. She supported us during the long hours of analyzing data

in a way that motivated us to go on. I think we can both say for sure that every copromotor should

work like Joke Schuermans did with us. We also want to thank Tanneke Palmans for the technical

support. We experienced many technical problems during the process of this study, but Mme

Palmans came up with a solution. We knocked her door several times and sometimes at very busy

moments, but she always made some time free to help us with our not always so intelligent

questions. Furthermore a great thanks to our family for the warming support during the at times

stressful year of testing, analyzing and writing. We could for example always use a car when

necessary and enjoy the waffles they made during the testing period. I, Joachim De Brabander, would

also like to thank someone special. Lauren was always ready to listen and motivate me during the

hard work. She even made time for me when she was on an exchange program in Madagascar, to

keep me go on and finish this project. This support is not always so self-evident and that is why I

really appreciate the things she has done for me. Last but not least, we (Jelle Bonte and Joachim De

Brabander) would like to thank each other. We were good friends before these 2 years of thesis but

now we are even closer friends. We both went on Erasmus and had a difficult time during our first

weeks back in Ghent. But we helped each other through these difficult moments while we had to

work at our thesis. We were a complementary team by knowing each other’s strong and weak

points. We literally spent weeks together in the chamber of data processing. But we motivated each

other by playing music at the right moment or knowing when to have to stop playing music, by

buying lunch for each other, by shout out our frustrations together … I, Jelle Bonte, could not have

wished a better friend/colleague to bring this thesis to a good end.

Table of contents

Figures and tables list…………………………………………………………………………………………………………………………5

List of used abbreviations………………………………………………………………………………………………………………..…6

Abstract ................................................................................................................................................... 7

Introduction ............................................................................................................................................. 9

Materials and Methods: ........................................................................................................................ 11

Participants ........................................................................................................................................ 11

Testing procedure ............................................................................................................................. 11

Data analysis ...................................................................................................................................... 13

Statistical analysis .............................................................................................................................. 14

Results ................................................................................................................................................... 15

Anthropometrics and injury characteristics ...................................................................................... 15

EMG-Data .......................................................................................................................................... 15

3D-kinematic data ............................................................................................................................. 16

Discussion .............................................................................................................................................. 19

Conclusion ............................................................................................................................................. 22

References ............................................................................................................................................. 22

Abstract in lekentaal…………………………………………………………………………………………………………………………27

Appendix………………………………………………………………………………………………………………………………………….28

Figures and tables list

Figure 1: Electrodes of internal and external oblique muscles…………………………………………………………12

Figure 2: Electrodes of the lumbar erector spinae……………………………………………………………………………12

Figure 3: Participant ready for sprint trials with 44 passive sensors and elastic cohesive bandage….13

Figure 4: Pelvis-thorax dynamics………………………………………………………………………………………………………17

Figure 5: Anterior tilting in the thorax in the injury group compared to the control group………………17

Figure 6: Hip joint angle at heelstrike……………………………………………………………………………………………….18

Figure 7: Greater hip ROM towards extension in control group compared to injury group……………..18

Figure 8: Knee joint angle at heelstrike…………………………………………………………………………………………….19

Table 1: Anthropometrics of both groups…………………….……………………………………………………………….….15

Table 2: Significant difference of lumbar erector spinae activity in front swing phase……………………..16

Table 3: Correlations between hamstring - and core muscle activity………………………………………………..17

List of used abbreviations

ant anterior

BF Biceps Femoris

CSA Cross sectional area

DTS Direct Transmission System

ECG ElectroCardioGram

EMG ElectroMyoGram

GM Gluteus Maximus

HSI Hamstring Strain Injury

IBM International Business Machines

IR InfraRed

JB Jelle Bonte

JDB Joachim De Brabander

JS Joke Schuermans

LES Lumbar Erector Spinae

LLT-

model Lower Limb Trunk-model

MRI Magnetic Resonance Imaging

MTU Motor Tensile Unite

MVC Maximal Volonturay Contraction

post posterior

ROM Range of Motion

rs spearman correlation

Sig. significance

SM SemiMambranosus muscle

SPSS Statistical Package for the Social Sciences

ST SemiTendinosus muscle

7

The role of core stability in sustaining high speed running

hamstring injuries in male soccer players

Abstract

Background Core stability and lumbo-pelvic control exercises have a considerable share in primary

and secondary prevention of hamstring injuries nowadays. Former research has suggested that

lumbo-pelvic muscle activity would have an important influence on the amount of hamstring stretch

and - loading. However, the exact role of the core and pelvic muscles in the occurrence and

sustaining hamstring strain injuries (HSI) in a population of soccer players has not clearly been

investigated yet.

Objectives To assess the quality and the quantity of lumbo-pelvic muscle functioning during a

maximal acceleration effort in male soccer players and to verify whether these muscle activation

patterns differ based on the presence or the absence of a hamstring injury history.

Study design Cross-sectional study

Methods 12 soccer players with a recent hamstring injury history (within 2 years) and 12 matched

controls performed several sprints, in which the maximal acceleration phase was used for analysis.

Lower limb and trunk 3D kinematics and EMG data from the lumbo-pelvic stabilizers and the

hamstring muscles were gathered within this phase. Prior to sprinting, MVC’s of each muscle were

measured. In the post hoc EMG and kinematic data analysis main focus oriented towards the results

in terminal swing phase, which appears to be the most susceptible phase for HSI in the running cycle.

Results The lumbar erector spinae muscle at both sides were significantly less active in the injured

group (96% of MVC) compared to the control group (192% of MVC)(p=0.030) during the front swing

phase of the involved leg. Injury history was able to predict over 20% (R2=0.203) of the variability

within the observed outcome on lumbar erector spinae muscle activity during front swing. (p=0.030).

At heel strike, the injury group demonstrated a significantly higher anterior thorax tilting (p=0.044)

and a tendency towards greater hip and knee flexion in comparison to the control group.

Conclusion The lumbar erector spinae could play a major role in the pathophysiology (and re-

occurrence) of HSI due to its function to control the forward flexion of the trunk and to maintain an

adequate vertebral position. The part of other core stability muscles in the mechanism of HSI was not

cleared out. Lumbo-pelvic (and lower limb) running kinematics most probably determine the soccer

player’s hamstring injury risk, however large scale prospective studies are required to confirm (and

identify the exact nature of) this hypothesis.

Keywords: hamstring strain / core stability / sprint / football / EMG

8

Achtergrond Core stability en lumbo-pelvische controle oefeningen hebben momenteel een

aanzienlijk aandeel in primaire en secundaire preventie van hamstringblessures. De literatuur

suggereert dat activiteit van de lumbo-pelvische spieren een belangrijke invloed zou hebben op rek

en belasting van de hamstrings. Maar de exacte rol van de stabiliserende romp –en bekkenspieren bij

het ontstaan en de recurrentie van een hamstringverrekking bij voetbalspelers is nog niet specifiek

onderzocht geweest.

Doelstellingen De kwaliteit en kwantiteit van lumbo-pelvische activiteit tijdens een maximale

versnelling onderzoeken bij voetbalspelers en hierbij verifiëren of de activeringspatronen van deze

spieren een belangrijk verschil vertonen bij aan- of afwezigheid van een eerder opgelopen

hamstringblessure.

Onderzoeksdesign Cross-sectionele studie

Methode 12 voetbalspelers die de voorbije 2 jaar een hamstringblessure opgelopen hebben en 12

spelers functionerend als controlegroep, hebben verscheidene sprints uitgevoerd, waarbij de fase

van maximale versnelling werd geanalyseerd. Zowel 3D kinematica van het onderste lidmaat en

romp als EMG gegevens van de lumbo-pelvische stabilisatoren en de hamstrings werden gemeten in

deze fase. Voor het sprinten, werden maximale willekeurige contracties (MWC’s) afgenomen. Bij

verwerking van de EMG en de kinematica gegevens lag de focus op de resultaten in de terminale

zwaaifase, die in de literatuur beschreven wordt als de meest provocatieve fase voor een

hamstringblessure.

Resultaten De lumbale erector spinae vertoonde beiderzijds significant minder activiteit in de

geblesseerde groep (96% van MWC) dan in de controlegroep (192% van MWC)(p=0.030) tijdens de

voorwaartse zwaaifase van het aangedane lidmaat. In deze fase kan een eerder opgelopen

hamstringblessure 20% (R2=0.203) van de variabiliteit in lumbale erector spinae activiteit voorspellen

(p=0.030). Bij hielcontact vertoonde de voorheen geblesseerde groep een significant hogere

voorwaartse verplaatsing van de romp en een tendens naar grotere heup - en knieflexie in

vergelijking met de controlegroep.

Conclusie De lumbale erector spinae zou op basis van deze resultaten een belangrijke rol toebedeeld

kunnen worden in het ontstaan en recurrentie van hamstringblessures als gevolg van zijn functie in

het controleren van voorwaartse rompflexie en in het behoud van een adequate positie van de

wervelkolom. Het aandeel van de andere stabiliserende bekken-en rompspieren in het mechanisme

van hamstringblessures kon aan de hand van deze studie niet verder verduidelijkt worden.

Waarschijnlijk bepaalt de lumbo-pelvische kinematica, net zoals de kinematica van het onderste

lidmaat, het risico op een hamstringblessure tijdens het sprinten bij voetbalspelers. Maar er is nood

9

aan grootschalige prospectieve studies om deze hypothese te staven en het exacte mechanisme

ervan te achterhalen.

Introduction

Hamstring injuries are one of the most common injuries in sports that include running and sprinting

such as soccer. Ekstrand et al. (2015)6 found an injury incidence of 8.0 injuries per 1000 h of exposure

in soccer. 12% of these injuries were hamstring injuries. Hamstring strain injuries (HSI) are the single

most predominant sports injuries, that also have the highest tendency to reoccur. J. Ekstrand (2011)5

reported a recurrence rate of 16%. In an attempt to decrease this high (re)injury incidence,

researchers have been investigating the risk factors (loss of eccentric hamstring strength 14,19, -

reduced H:Q ratio 3,28, -asymmetrical power of the hamstrings 7,16, -reduced flexibility 10,27, -previous

hamstring injury 8,15,25, previous knee injury 25, Aboriginal race 25, motor control 3, fatigue 9,23 and age

8,10,15,25 ) -and the underlying injury mechanisms. Soccer players tend to injure their posterior thigh

region the most during explosive running and kicking activities. In terms of this injury mechanism,

previous research has demonstrated that the hamstrings are most vulnerable for strain injuries in the

terminal swing phase of the running cycle. Previous research has already demonstrated that

predominantly the lateral hamstring, the long head of the biceps femoris (BF), seems to be subject of

strain or rupture, whereas the medial hamstrings, semitendinosus (ST) and semimembranosus (SM),

are less frequently injured.

Researchers took into account the influence of running kinematics and hamstring function during

sprinting, to explain why the hamstring are most susceptible for strain injuries during specifically the

terminal swing phase of the running cycle. The hamstrings reach their maximum length during the

terminal swing phase24, where they also demonstrate maximal activity4. The hamstrings also have to

work eccentrically during the front swing phase, with a rapid conversion to efficient concentric

contraction in the early stance phase, for adequate propulsion29. The eccentric work and the high

amounts of muscle stretch during the terminal swing phase, are two major factors that most

probably contribute to the susceptibility for strain injuries seen in the hamstrings.

The lateral Biceps BF (and in particularly the long head) is more susceptible to strain injuries than the

medial hamstring muscles. Former research has been trying to explain this location specific injury

occurrence by investigating the exact muscle mechanics and loading characteristics of the 3 bi-

articular hamstring bellies in sprinting.

10

From these findings we conclude that the hamstring muscles are most susceptible to contraction-

induced damage (cf. explosive running and kicking related muscle injuries) when they are activated

and lengthened simultaneously. An active MTU stretch of 5% can already be sufficient to cause

damage to the muscle2. The hamstring muscles show the largest stretch at the point where they have

to work eccentrically. This point corresponds with the terminal swing phase, as illustrated above.

Based on the exact nature of this (eccentric) effort-related injury mechanism, protecting the

hamstring muscle against strain injury would require providing the muscle complex with (1) maximal

explosive strength capacity and (2) sufficient stretching tolerance, whilst protecting the muscle-

tendon unit against excessive stretch and strain loading throughout the running cycle. The amount of

tensile stretch/stress placed upon the muscle unit is dependent on several factors. There might be an

important influence of the lumbo-pelvic muscles in the stretch on the hamstring muscles4, next to

fatigue12,22 and increasing speed18. But the exact role of the core and pelvic muscles in the occurrence

and sustaining HSI in a population of soccer players has not clearly been investigated yet.

However, there are some findings that may indicate that a rehabilitation program including core

stability has better outcomes in terms of HSI re-injury 21 and that injuries of the lower extremity

could be predicted by taking into account the endurance capacity of the core muscles26 and the size

of the lumbar erector spinae (LES) muscle11.

The hamstring muscles are phasic mobilizing muscles with a primary dynamic function in locomotion.

(concentric effort during stance - and backswing phases, eccentric effort during front swing phase)

Due to their anatomy and topography however, the hamstring muscles can also contribute to pelvic

control and stability through isometric and bilateral activity. Because of their morphology, this

stabilizing function is only a side issue and certainly no key feature within their primary task. That is

why, to our opinion, a lack of core stability and lumbo-pelvic control during sprinting, could increase

the biomechanical demands placed on the hamstring muscles, which could result in overload.

We assume that the function of core stability might play a major role in the occurrence of HSI. Up

until now, prospective studies have only been focusing on analytical core muscles functioning,

without assessing the core muscle integrity during functional and dynamic sports activities. However,

more information about the function of the core muscles during sprinting is necessary to determine

the exact role of the core muscles in the occurrence of HSI in soccer. That is why the main objective

of this study is to assess the quality and the quantity of lumbo-pelvic muscle functioning during a

maximal acceleration effort in a population at risk (male soccer players) and to verify whether these

muscle activation patterns differ based on the presence or the absence of a hamstring injury history.

11

In this cross-sectional study, we will specifically focus on the activity of the lumbo-pelvic (“core

stability”) muscles and the 3D movement of the core and pelvis in the terminal swing phase of

sprinting (cf. injury mechanism). By comparing the exact electromyographic activation features of the

stabilizing muscles and the kinematic data of the core and pelvis regions between a group with a

history of HSI and a healthy matched control group, we hope to gain some understanding in the

exact role of “core stability” in the predominant hamstring injury mechanism.

Materials and Methods

Participants

From February to May 2014, 24 players from several Belgian soccer clubs were recruited via

physiotherapists, osteopaths and trainers. All recruited players met the inclusion criteria: male

players participating in Belgian soccer competition, aged between the limits of 18 and 35, member of

a soccer club, and for the injury group, reporting having sustained a significant hamstring injury

somewhere within the 2 last seasons, preventing the athlete to participate in training or match play

for at least one entire week. Participants were excluded if they reported an important knee or hip

injury in their medical history, which could have influenced their running pattern and biased our

results. Ultimately, all 24 soccer players were included, of which 12 players with a recent hamstring

injury history and 12 matched controls. All participants did not have any complaints or restriction to

play at the moment of testing. Written informed consent statements were obtained after

participants had read the volunteer information papers.

Testing procedure

The entire testing was performed during the first two weeks of July as well as the last week of August

2015 and took place in “Topsporthal Vlaanderen”(Ghent, Belgium). Prior to testing, each participant

was thoroughly informed about the content and the purpose of the testing procedure and was asked

to sign Informed Consent and to complete a questionnaire (injury history, foot dominance,

competition level, field position, possible current injuries …). After taking care of the administration,

the participants were instructed to perform a standardized 10 min warming up session, during which

they were instructed to run along the central running track at a comfortable pace, while sporadically

doing several explosive accelerations towards maximal sprinting velocity. Next, subject preparation

was commenced. We gathered 3D kinematics of the lower limb and trunk as well as EMG data from

12

the lumbo-pelvic stabilizers and the hamstring muscles. For the kinematic analysis, Qualisys

hardware devices (8 IR Oquus cameras and 44 passive markers) and homonymous software package

were attributed (Qualisys Motion Capture Systems, Qualysis AB, Gothenburg, Sweden). For the EMG

testing procedure, the wireless 16 channel Noraxon DTS (Direct Transmission System) was used

(Velamed GmbH, Köln, Germany).

When the participant finished his warming up session, the researchers began with the electrode

placement for the Maximal Voluntary Contraction capacity (MVC) procedure. After skin preparation

(shaving, scrubbing and cleaning), a total number of 32 Ag/AgCl pre-gelled electrodes were placed on

the muscles of the lower limb and trunk: internal and external obliques, LES, gluteus maximus (GM),

ST, SM and BF (figure 1 and 2). The SENIAM guidelines were used for standardized electrode

placement (Surface Electromyography for the Non-Invasive Assessment of Muscles). An elastic

cohesive bandage was attached around the participant’s trunk to stabilize the electrodes and the DTS

amplifiers. After electrodes and amplifiers were carefully put in place, MVC was determined for each

of the above mentioned muscles, which allowed us to normalize the activity signal evoked during

dynamic sprinting task during data analysis. Each MVC was held for 5 seconds. External resistance

was systematically provided by the same qualified assessor (JDB). Every muscle was tested three

times, with a little break of 15 seconds in between repetitions.

After completing the MVC assessment, the 44 passive sensors of the Qualisys system were placed on

the trunk and lower limb of the participant (figure 3 and appendix). For this kinematic testing

procedure and the post-hoc analysis, the LLT model was used. (Jos Van Renterghem, John Moores

University, Liverpool, UK). Before the sprint trials, one static trial and four ‘functional joint’ trials

were captured (functional hip- and knee-joint trials for the left and right legs). This static

measurement as well as the ‘functional joint’ measurements, which were needed to accurately

Figure 1: electrodes of internal

and external oblique muscles

Figure 2: electrodes of the

lumbal erector spinae

13

determine the rotational axis of the knee- and hip joints in each individual, are required for the

assembly of a virtual model, to which the kinematic data during full sprint could be scaled during

data analysis. After capturing the static and functional joint trials, 3D kinematic analysis and EMG-

recording of the hamstring and lumbo-pelvic muscles were performed in between meter 15 and 20

of a 35 meter sprinting track, which is an optimal distance to reach maximal acceleration without

risking injuries. There were no kinetic measurements. The sprint trial had to be maximal and was only

accepted if a full stride was measured by the Optogait system (Microgate, Italy) which was necessary

for processing. Because no kinetic data were measured, the use of the Optogait system was essential

for stance- and swing phase differentiation. Finally, 6 clean left and right strides were captured

within the Qualisys, Noraxon DTS and Optogait software packages. The entire testing procedure was

performed by the same researchers (JS, JB, JDB) which minimized the risk of inter-tester bias. This

study was approved by the Ethics Committee of the Ghent University Hospital (number of approval:

EC/2013/118).

Data analysis

The EMG data were processed using the MR3.6 software (Noraxon). The MVC-signals were corrected

for ECG interference, rectified and smoothed within a 20ms window. The EMG signals, captured

during the sprints, were corrected for ECG signal, high-pass filter at 20Hz, rectified and smoothed

within the same 20ms window. For each stride, we focused on the bilateral internal and external

oblique, the bilateral LES and the contralateral GM, ST and BF. For the left stride (left toe off to left

heelstrike) for example, we assessed the entire core as well as the GM and hamstring muscles of the

right leg.

Figure 3: participant ready for

sprint trials with 44 passive sensors

and elastic cohesive bandage

14

The 3D data of the sprint trials and static trials were processed by using the Qualisys and Visual 3D

(C-Motion, Germantown, USA) software packages. All markers were identified and the sprint trials

were cropped to 1 stride within the Qualisys Track Manager interface. These trials were transferred

to C3D files for segment and joint angle calculation during swing and stance in Visual 3D (C-Motion).

We specifically focused on lower limb and trunk kinematics (with primary attention to pelvis

kinematics) in transversal, frontal and sagittal planes during terminal swing and initial stance phases

of the sprinting cycle.

Statistical analysis

When creating the general database of all kinematic and EMG data during sprinting, we replaced ‘left

and right side’ kinematics and muscle activation patterns with 3D and EMG characteristics of the

‘involved and non-involved body-sides’. In this way, we could combine all injured sides at once

without having to take into account if a right or left stride was recorded. Determination of which side

was involved or noninvolved in the control group, was randomly done by assessing the percentage of

dominant side injuries in the injury group (63%) and including the same amount of dominant

(respectively non-dominant legs) in the control group, for in-between-group comparison. First of all,

descriptive statistics were attributed to assess the distribution of the data (normality testing) and

getting a general overview of means and standard deviations of the anthropometric data and the

kinematic and EMG-related outcome variables.

For the EMG-data analysis, only the MVC corrected signals were used. Statistical analysis of the EMG-

data was focused on the muscle activation patterns during specifically the front swing phase of the

involved side. To check for in-between-group differences in front-swing related muscle activity, the

independent students t-test or the Mann-Whitney U test was used. Afterwards, possible linear or

logistic associations between injury history and running related muscle activity was evaluated.

Possible correlations between the activity features of the hamstring muscles and those of the core

and pelvis muscles were also assessed, using the Spearman and Pearson correlation coefficients. The

same procedure was performed for the statistical analysis of the kinematic data. An independent

samples student t-test was used to examine possible in-between-group differences in joint angles

(knee, hip, pelvis and thorax) at the moment of touch down (primary ground contact) or in Joint

Range of Motion throughout the entire stride. Data analysis was done with the SPSS V.22 Statistical

Software package (IBM Corp. New York, USA), and the level of significance was set at α=0.05.

15

Results

Anthropometrics and injury characteristics

Anthropometrics of both groups can be found in table 1. There were no significant differences found

between the 2 groups .

EMG-Data

The LES at the side of the previously injured hamstring, was significant less active in the injured group

(96% of MVC) than in the control group (192% of MVC)(p=0.030) during the front swing phase of the

involved leg (Table 2). Nonparametric testing revealed that the LES at the noninvolved side is also

significantly less active during this frontswing phase (with the homonymous leg being in backswing

phase at that moment). There were no significant differences for the amount of abdominal muscle

activity, GM activity or hamstring muscle activity during this frontswing phase, nor did we find in-

between-group differences in muscle activity during stance- or backswing phases.

Regression analysis revealed that injury history was able to predict over 20% (R2=0.203) of the

variability within the observed outcome on LES activity during front swing. (p=0.030)

Contralateral LES activity (corresponding the non-injured side or non-involved side) was significantly

correlated with ST (p=0.033, rs= 0.673) and BF muscle activity in the injury group ( p=0.043,

rs=0.618), but not in the control group. Finally, GM activity in the involved side was significant

correlated with BF activity, but not with ST activity, in both groups. Other less important correlations

between hamstring- and core muscle activity can be found in table 3.

CONTROL INJURY

weight 77,4 +-6,1 74,5+-7,1

height 1,84+-0,1 1,81+-0,1

BMI 22,9+-1,4 22,8+-1,7

age 23,0+-3,9 25,0+-3,5

Table 1: Anthropometrics of both groups (mean +- standard deviation)

16

Levene's Test

for Equality of

Variances t-test for Equality of Means

F Sig. t df

Sig.

(2-

tailed)

Mean

Difference

Std. Error

Difference

95% Confidence Interval

of the Difference

Lower Upper

MU_I_FS_

NONINVOLVED

STRIDE_MVC

Equal

variances

assumed

,292 ,596 2,361 17 ,030 ,96001857 ,40654111 ,10229180 1,81774533

Equal

variances

not

assumed

2,280 13,148 ,040 ,96001857 ,42111744 ,05129150 1,86874563

control group:

independent Muscle Correlation coefficient p-value

biceps femoris (front swing) gluteus maximus 0.881 0.004

semitendinosus 0.810 0.015

semitendinosus (front swing) Internal Oblique injured side

0.905 0.002

biceps femoris 0.810 0.015

Injured group:

biceps femoris (front swing) iliocostales thoracicus injured side

-0.627 0.039

Lumbar erector spinae noninjured side

0.618 0.043

external oblique non-injured side

0.827 0.002

Internal oblique injured side

0.782 0.004

gluteus maximus 0.827 0.002

semitendinosus Lumbar erector spinae non-injured side

0.673 0.033

external oblique non-injured side

0.636 0.048

interne oblique injured side

0.661 0.038

Table 2: Significant difference of Lumbal erector spinae activity in front swing phase

(significant values are highlighted in blue).

Table 3: correlations between hamstring - and core muscle activity

17

3D-kinematic data

The injury group presented significantly less pelvis-thorax dynamics in the sagittal plane throughout

the front swing in sprinting, with an average Range of Motion of 8.5° versus 11.3° in the control

group. (figure 4)(p=0.018) Furthermore, the amount of anterior tilting in the thorax (in reference to

the pelvis position) at the moment of heelstrike of the involved leg, was significantly greater in the

injury group compared to the control group (mean difference of 6.3°, p=0.044) (Figure 5).

Figure 4: Pelvis-thorax dynamics (red =injured group; grey = control group)

Figure 5: anterior tilting in the thorax in the injury group

compared to the control group (p=0.044)

18

These findings indicate a more rigid thorax-pelvis coordination pattern/interplay tilt pattern during

the front swing phase, resulting in a more pronounced flexion in the lumbo-pelvic joints at the

moment of heel strike in the formerly injury group, compared to the control group. In terms of the

hip and knee joint angles, the injury group presented the tendency towards greater flexion range of

motion in the hip joint (-48.35643577) than the control group (-43.54561406) at heel strike (Figure 6

and 7). At knee joint level, the control group presented a tendency towards larger extension joint

angle than the injury group at heel strike (Figure 8).

Figure 6: Hip joint angle at heelstrike

Figure 7: greater hip ROM towards extension in control group

compared to injury group. (red =injured group; grey = control group)

19

Discussion

As stated in the introduction it is commonly known that the pathophysiology of HSI exists of a high

eccentric hamstring muscle loading while being stretched simultaneously. In this study, several

interesting kinematic and EMG characteristics were found that could be associated with a history of

hamstring injuries and highlight the importance of adequate running kinematics and corresponding

muscle activity in hamstring injury risk reduction.

First of all, a significantly smaller pelvic forward-backward rotation ROM was found in the injury

group. Taking into account that the front swing phase in sprinting induces a backward rotation of the

pelvis because of the considerable amount of hip flexion in this phase, the establishment of

significantly more pronounced anterior rotation of the pelvis in the injury group during this phase,

indicates the existence of a maladaptive movement strategy, inducing even higher levels of muscle

tendon stretch on the already heavy loaded hamstring complex. Next to this increased anterior

rotation of the pelvis compared to the control group, the tendency towards a higher hip flexion ROM

during the terminal swing phase of sprinting in the injury group, might also induce elevated muscle

stretch and excessive loading on the already weakened hamstring unit, possibly increasing the risk of

re-injury. The kinematic findings in the injury group, possibly evoking greater stretch on the

Figure 8: Knee joint angle at heelstrike

20

hamstrings muscles could be explained by multiple causes. First, we also found that the LES muscles

are significantly less active in terminal swing phase of sprinting in the injury group, compared to the

control group. A lack of eccentric activity of the LES muscles could lead to the more forward flexed

trunk position during sprinting, also seen in the injury group. Secondly, the iliopsoas muscle could

play a major role in these altered running kinematics after hamstring injury. Chumanov et al (2007)4

showed that an excessively active iliopsoas muscle during the double float phase of running, can

significantly increase hamstring muscle-tendon stretch. This muscle induces hip flexion and a small

amount of knee extension of the opposite leg (myofascial chains), which both increases hamstring

stretch. This iliopsoas tightness or hyperactivity could also explain the greater hip flexion in the injury

group. However, not only an excessively active or tight Iliopsoas can cause increased hamstring

loading, also active weak or fatigued iliopsoas muscle can cause increased pelvic tilting and

decreased lumbo-pelvic control 22.

If we consider the LES as a stabilizing muscle of the spine, the function of the LES is not only

controlling the forward flexion of the trunk with an eccentric contraction, but also keeping the spine

in a correct and stable position while moving. We found that the LES is less active during the terminal

swing phase in the injury group. If we take into account that a hyperactive or tight iliopsoas muscle,

as mentioned in the study of Chumanov et al. (2007)4, acts on the spine during airborne phase, in

which the lumbo-pelvic complex is fairly unstable, it seems very plausible that the iliopsoas can cause

excessive forward tilted position of the pelvis as well as a more forward flexed position of the trunk,

as it has to compensate for LES deficiency.

We also found a tendency of greater knee flexion at heel strike in the injury group. This can be seen

as a compensation strategy for the greater anterior tilt of the pelvis and the tendency of greater hip

flexion at the moment of heel strike in the injury group. This strategy could be sufficient for the

medial hamstring muscles but the lateral hamstring muscles can still experience a stretch since the

BF has a smaller knee flexion moment arm compared to the medial hamstrings1. As a consequence of

this potential compensation strategy, the BF experiences an earlier stretch than the medial

hamstrings during sprinting. This would explain the results of Higashira et al.(2010)12, who found that

the lateral hamstring muscles are active earlier than the medial hamstrings and Schache et al.

(2013)18 who found that too early activation of the BF during forward swing would be one of the

mechanisms of lateral HSI. In this aspect, Schuermans et al.(2014)20 found that there is more

symmetrical activity between the lateral and medial hamstring muscles after injury, what indicates a

change in neuromuscular control between the hamstring bellies. This causes a less efficient

contraction, decrease in pH and an earlier fatigue. The authors mention that the ST would be less

21

resistant to a pH changes, which would oblige the BF to compensate for the lack of endurance of the

ST. The BF itself would be less resistant to stretch and high negative work during the terminal swing.

If the hamstring muscles have to compensate for a greater anterior pelvis tilting with simultaneously

altering knee kinematics, the eccentric load on the hamstrings increases and starts earlier

throughout the swing phase. This possibly causes excessive muscle loading and earlier onset of

fatigue, which might imply a greater risk of HSI. Besides, LES deficiency during sprinting not only

increases muscle stretch, but forces the hamstrings to collaborate in the maintenance of lumbo-

pelvic stability in running, for which it is not morphologically nor metabolically suited. This could

possibly explain why the smaller pelvis range of motion is less in the injury group, as mentioned

above. In this way, the hamstrings could restrict pelvic ROM because in an attempt to adequately

stabilizing the lumbo-pelvic region, next to their phasic propulsion function around the hip and knee

joints. This could be another explanation of the compensation at knee level.

For all other core muscles, we could not find any significant differences in EMG activity for other core

muscles, based on injury history. Although, Chumanov and colleagues (2007)4 showed that the

internal oblique muscles have an important role in decreasing the stretch of the BF muscle, we could

not find any differences in activity of the obliques between both groups.

Limitations and recommendations for future research

There are a number of limitations that should be considered while interpreting the results of this

study. First of all, due to a small sample size, the power of this study may be too low to make some

generalized conclusions for all soccer players. Secondly, the consecutive sprints were performed with

only a short resting period in between. Increased fatigue could influence the sprinting mechanics and

mean EMG activity of the measured muscles. Morin et al (2012)13 only mention a decrease in

maximum strength, but no changes in running patterns/mechanics in high intensity sprint fatigue,

which places this possible limitation into perspective. On the other hand, soccer players also

experience fatigue during competition or training on the soccer field, so presence of fatigue might

make this sprinting analysis even more specific and sensitive to possible injury related adaptations.

Furthermore, taking in account the major role of the iliopsoas muscle in our discussion, the

significant results of this study could be better interpreted if we also disposed of the EMG activity of

the iliopsoas and the quadriceps muscle during the sprinting trials. Besides, to our opinion, the role

of the diaphragm in core stabilization and spinous alignment has to be investigated more thoroughly.

Next, determining muscle force from EMG data is not a straightforward process, particularly for

22

sprinting. It is influenced by muscle length, muscle fatigue, contraction type, contraction velocity and

the amount of contribution provided by synergistic muscles 17. In contrary to muscle functional MRI,

we could not measure solitary the pars profundus of the multifidus muscle due to crosstalk. This is

why we preferred to use the LES as term instead of multifidus lumbalis in this article. The effect of

crosstalk is minimalized by standardizing the placement of electrodes in both groups and by

comparing the results of both groups. Finally, there has to be the consideration if a straight, clean

sprinting trial is representative for a soccer related hamstring injury. Soccer players have to change

directions all the time and ball manipulation during sprinting could lead to substantially different

trunk mechanics than those investigated in this study.

Conclusion

From this discussion we can conclude that the LES possibly plays a major role in the pathophysiology

(and re-occurrence) of HSI due to its function to control the forward flexion of the trunk and to

maintain an adequate vertebral position. We found that the LES, is significantly less active during the

terminal swing phase of the running cycle in the formerly injured group. These results correspond

with Hides et al.(2011)11, who showed that smaller cross sectional area’s (CSA) of the multifidus

lumbalis muscle at L5 levels and a smaller CSA and disfunction of the multifidus lumbalis at L3 and L4

levels can predict injuries of the groin, hip or thigh. This could mean that multifidus lumbalis

inactivity and/or disfunction is directly correlated with HSI. This study revealed that injury history was

able to predict over 20% (R2=0.203) of the variability within the observed outcome on LES muscle

activity during front swing (p=0.030). The role of the other core stability muscles, such as internal and

external obliques, GM and diaphragm in the mechanism of HSI during sprinting was not cleared out.

Further research is necessary to identify the role of the stabilizing core muscles (both separately and

in functional cocontraction) in prevention of sprinting related hamstring injuries in soccer players.

References

1) Buford, W., F. Martey Ivey, D. Malone, et al. Muscle balance at the knee: moment arms for the

normal knee and the ACL-minus knee. 1997 Dec. IEEE Trans. Rehabil. Eng; 5(4) :367–379.

2) Butterfield TA, Herzog W. Quantification of muscle fiber strain during in vivo repetitive stretch-

shortening cycles. J Appl Physiol. 2005 Aug; 99(2):593–602

23

3) Cameron M, Adams R, Maher C. Motor control and strength as predictors of hamstring injury in

elite players of Australian football. 2003 Nov; 4(4): 159-166

4) Chumanov ES1, Heiderscheit BC, Thelen DG. The effect of speed and influence of individual

muscles on hamstring mechanics during the swing phase of sprinting. J Biomech. 2007;40(16):3555-

62. Epub 2007 Jul 19.

5) Ekstrand J1, Hägglund M, Waldén M. Epidemiology of muscle injuries in professional football

(soccer). Am J Sports Med. 2011 Jun;39(6):1226-32.

6) Ekstrand J, Hägglund M, Waldén M. Injury incidence and injury patterns in professional football

the UEFA injury study Within the soccer scene. Br J Sports Med. 2011 Jun;45(7):553-8.

7) Fousekis K1, Tsepis E, Poulmedis P, Athanasopoulos S, Vagenas G. Intrinsic risk factors of non-

contact quadriceps and hamstring strains in soccer: a prospective study of 100 professional players.

Br J Sports Med. 2011 Jul;45(9):709-14

8) Gabbe BJ1, Bennell KL, Finch CF, Wajswelner H, Orchard JW. Predictors of hamstring injury at the

elite level of Australian football. Scand J Med Sci Sports. 2006 Feb;16(1):7-13.

9) Greig M1, Siegler JC. Soccer-specific fatigue and eccentric hamstrings muscle strength. J Athl Train.

2009 Mar-Apr;44(2):180-4

10) Henderson G1, Barnes CA, Portas MD. Factors associated with increased propensity for hamstring

injury in English Premier League soccer players. J Sci Med Sport. 2010 Jul;13(4):397-402

11) Hides JA, Brown CT, Penfold L, Stanton WR. Screening the lumbopelvic muscles for a relationship

to injury of the quadriceps, hamstrings, and adductor muscles among elite Australian Football League

players. J Orthop Sports Phys Ther. 2011 Oct;41(10):767-75.

12) Higashihara A1, Ono T, Kubota J, Okuwaki T, Fukubayashi T. Functional differences in the activity

of the hamstring muscles with increasing running speed. J Sports Sci. 2010 Aug;28(10):1085-92.

24

13) Morin JB, Tomazin K, Samozino P, Edouard P, Millet GY. High-intensity sprint fatigue does not

alter constant-submaximal velocity running mechanics and spring-mass behavior. Eur J Appl Physiol.

2012 Apr; 112(4): 1419-28.

14) Opar D1, Williams M, Timmins R, Hickey J, Duhig S, Shield A. Eccentric hamstring strength during

the nordic hamstring exercises is a risk factor for hamstring strain injury in elite Australian football: a

prospective cohort study. Br J Sports Med. 2014 Apr;48(7):647-8

15) Orchard JW. Intrinsic and extrinsic risk factors for muscle strains in Australian football. Am J

Sports Med. 2001 May-Jun;29(3):300-3.

16) Schache AG1, Crossley KM, Macindoe IG, Fahrner BB, Pandy MG. Can a clinical test of hamstring

strength identify football players at risk of hamstring strain? Knee Surg Sports Traumatol Arthrosc.

2011 Jan;19(1):38-41.

17) Schache AG, Dorn TW, Blanch PD, Brown NA, Pandy MG. Mechanics of the human hamstring

muscles during sprinting. Med Sci Sports Exerc. 2012 Apr; 44(4):647-58.

18) Schache AG1, Dorn TW, Wrigley TV, Brown NA, Pandy MG. Stretch and activation of the human

biarticular hamstrings across a range of running speeds. Eur J Appl Physiol. 2013 Nov;113(11):2813-

28.

19) Schmitt B, Tim T, McHugh M. Hamstring injury rehabilitation and prevention of reinjury using

lengthened state eccentric training: a new concept. Int J Sports Phys Ther. 2012 Jun;7(3):333-41.

20) Schuermans J, Van Tiggelen D, Danneels L, et al. Biceps femoris and semitendinosus—teammates

or competitors? New insights into hamstring injury mechanisms in male football players: a muscle

functional MRI study. Br J Sports Med 2014; 48: 1599-1606

21) Sherry MA1, Best TM. A comparison of 2 rehabilitation programs in the treatment of acute

hamstring strains. J Orthop Sports Phys Ther. 2004 Mar;34(3):116-25.

22) Small K1, McNaughton LR, Greig M, Lohkamp M, Lovell R. Soccer fatigue, sprinting and hamstring

injury risk. Int J Sports Med. 2009 Aug;30(8):573-8.

25

23) Small K1, McNaughton L, Greig M, Lovell R. The effects of multidirectional soccer-specific fatigue

on markers of hamstring injury risk. J Sci Med Sport. 2010 Jan;13(1):120-5.

24) Thelen DG1, Chumanov ES, Hoerth DM, Best TM, Swanson SC, Li L, Young M, Heiderscheit BC.

Hamstring muscle kinematics during treadmill sprinting. Med Sci Sports Exerc. 2005 Jan;37(1):108-14.

25) Verrall GM1, Slavotinek JP, Barnes PG, Fon GT, Spriggins AJ. Clinical risk factors for hamstring

muscle strain injury: a prospective study with correlation of injury by magnetic resonance imaging. Br

J Sports Med. 2001 Dec;35(6):435-9.

26) Wilkerson GB1, Giles JL, Seibel DK. Prediction of core and lower extremity strains and sprains in

collegiate football players: a preliminary study. J Athl Train. 2012 May-Jun;47(3):264-72.

27) Witvrouw E1, Danneels L, Asselman P, D'Have T, Cambier D. Muscle flexibility as a risk factor for

developing muscle injuries in male professional soccer players. A prospective study. Am J Sports

Med. 2003 Jan-Feb;31(1):41-6.

28) Yeung SS1, Suen AM, Yeung EW. A prospective cohort study of hamstring injuries in competitive

sprinters: preseason muscle imbalance as a possible risk factor. Br J Sports Med. 2009 Aug;43(8):589-

94

29) Yu B1, Queen RM, Abbey AN, Liu Y, Moorman CT, Garrett WE. Hamstring muscle kinematics and

activation during overground sprinting. J Biomech. 2008 Nov 14;41(15):3121-6.

Abstract in lekentaal

Achtergrond Buikspieren, spieren rond het bekken en spieren ter hoogte van de lage rug worden gezien als belangrijke stabilisatoren van romp, bekken en zelfs het onderste lidmaat. Hun functie is daarom van kapitaal belang voor veilig dagdagelijks en sportief bewegen. Daarenboven zouden deze spieren een invloed hebben op de hoeveelheid rek die de achterste dijspieren (hamstrings) te verduren krijgen tijdens het sprinten. Hoe meer rek op de spier, hoe groter de kans op blessure. Dergelijke hamstring blessure is de meest voorkomende sportblessure bij voetballers. De exacte rol van deze stabiliserende spieren in het blessuremechanisme van de hamstrings is nog niet echt aangetoond in de literatuur. Doelstellingen De activiteit van de stabiliserende spieren onderzoeken bij voetballers tijdens het uitvoeren van een maximale loopversnelling en hierbij nagaan of de activiteit van de stabiliserende spieren verschillend is naargelang aan-of afwezigheid van een eerder opgelopen hamstringblessure . Methode 12 voetbalspelers met een recent hamstring blessure verleden en 12 gezonde controles (spelers met zelfde lichaamsbouw en actief op hetzelfde competitieniveau), voerden verscheidene maximale versnellingen uit. Tijdens het sprinten hebben we enerzijds driedimensionale bewegingen van de benen en de romp, en anderzijds de spieractiviteit van de hamstrings en de stabiliserende spieren gemeten. Bij de verwerking van de resultaten lag de focus op driedimensionale informatie en de spieractiviteit tijdens de voorste zwaaifase van de loopcyclus, aangezien de hamstrings in deze fase de meeste rek moeten tolereren en hier zodoende ook het meest kwetsbaar zijn. Resultaten Een van de belangrijkste diepe stabiliserende spieren die achteraan tegen de wervelkolom ligt (lumbale erector spinae), wordt duidelijk minder geactiveerd bij de voorheen geblesseerde personen dan bij de controlegroep bij de fase van het volledig naar voor gezwaaide been. Wanneer het naar voor gezwaaide been grondcontact maakt met de hiel, dan vertoont de voorheen geblesseerde groep een duidelijk hogere voorwaartse buiging van de romp (wat meer rek op de hamstrings teweegbrengt) en wordt de heup en knie meer geplooid dan bij de controlegroep. Conclusie Het feit dat bovenstaande diepe stabiliserende spier minder actief is als je al een hamstringblessure hebt gehad, zou erop kunnen wijzen dat ze een belangrijke rol speelt in het ontstaan en het opnieuw oplopen van een hamstringblessure. Door te weinig activiteit kan deze spier de voorwaartse buiging van de romp niet voldoende controleren, waardoor de hamstring meer op rek komt en dus meer risico loopt op blessure. Bovendien heeft deze spier door zijn diepe ligging tegen de wervelkolom een zeer belangrijk aandeel in het behouden van een adequate positie van de wervelkolom tijdens het sprinten. Het aandeel van de andere stabiliserende buik-, rug- en bekkenspieren in het mechanisme van de hamstringblessures kon aan de hand van deze studie niet verduidelijkt worden. Looptechniek en degelijke controle van lage rug en bekken tijdens sprinten, zijn hoogst waarschijnlijk essentieel in het voorkomen van hamstringblessures binnen de voetbalsport. Toekomstig, grootschalig onderzoek is noodzakelijk om deze hypothese te staven. Sleutelwoorden: hamstring strain/ core stability/ sprint/ soccer/ EMG

Appendix

LLT-model

Trunk segment (4+2)

Marker name Description

C7 C7

STERNUM Sternum

XIP_PROC Xiphoid Process

T8 T8

ACROM_L Acromion Left

ACROM_R Acromion Right

Lower body (30+8)

ASIS_L Anterior Sacral Iliac Crest Left

PSIS_L Posterior Sacral Iliac Crest Left

ILCREST_L Iliac Crest Left

GTROC_L Greater Trochanter Left

ASIS_R Anterior Sacral Iliac Crest Right

PSIS_R Posterior Sacral Iliac Crest Right

ILCREST_R Iliac Crest Right

GTROC_R Greater Trochanter Right

UL_PR_ANT_L Upper Leg Proximal Anterior Left

UL_PR_POST_L Upper Leg Proximal Posterior Left

UL_DI_ANT_L Upper Leg Distal Anterior Left

UL_DI_POST_L Upper Leg Distal Posterior Left

KNEE_MED_L Knee Medial Epicondyle Left

KNEE_LAT_L Knee Lateral Epicondyle Left

LL_PR_ANT_L Lower Leg Proximal Anterior Left

LL_PR_POST_L Lower Leg Proximal Posterior Left

LL_DI_ANT_L Lower Leg Distal Anterior Left

LL_DI_POST_L Lower Leg Distal Posterior Left

MAL_MED_L Maleolus Medial Left

MAL_LAT_L Maleolus Lateral Left

HEEL_L Heel Left

MTH1_L Metatarsal Head 1 Left

MTH5_L Metatarsal Head 5 Left

UL_PR_ANT_R Upper Leg Proximal Anterior Right

UL_PR_POST_R Upper Leg Proximal Posterior Right

UL_DI_ANT_R Upper Leg Distal Anterior Right

UL_DI_POST_R Upper Leg Distal Posterior Right

KNEE_MED_R Knee Medial Epicondyle Right

KNEE_LAT_R Knee Lateral Epicondyle Right

LL_PR_ANT_R Lower Leg Proximal Anterior Right

LL_PR_POST_R Lower Leg Proximal Posterior Right

LL_DI_ANT_R Lower Leg Distal Anterior Right

LL_DI_POST_R Lower Leg Distal Posterior Right

MAL_MED_R Maleolus Medial Right

MAL_LAT_R Maleolus Lateral Right

HEEL_R Heel Right

MTH1_R Metatarsal Head 1 Right

MTH5_R Metatarsal Head 5 Right

Bold markers were removed after the static trials.